Date Published: April 12, 2019
Publisher: Public Library of Science
Author(s): Dmitrii I. Todorov, Robert A. Capps, William H. Barnett, Elizaveta M. Latash, Taegyo Kim, Khaldoun C. Hamade, Sergey N. Markin, Ilya A. Rybak, Yaroslav I. Molkov, Genela Morris.
Motor adaptation to perturbations is provided by learning mechanisms operating in the cerebellum and basal ganglia. The cerebellum normally performs motor adaptation through supervised learning using information about movement error provided by visual feedback. However, if visual feedback is critically distorted, the system may disengage cerebellar error-based learning and switch to reinforcement learning mechanisms mediated by basal ganglia. Yet, the exact conditions and mechanisms of cerebellum and basal ganglia involvement in motor adaptation remain unknown. We use mathematical modeling to simulate control of planar reaching movements that relies on both error-based and non-error-based learning mechanisms. We show that for learning to be efficient only one of these mechanisms should be active at a time. We suggest that switching between the mechanisms is provided by a special circuit that effectively suppresses the learning process in one structure and enables it in the other. To do so, this circuit modulates learning rate in the cerebellum and dopamine release in basal ganglia depending on error-based learning efficiency. We use the model to explain and interpret experimental data on error- and non-error-based motor adaptation under different conditions.
Motor learning is a process of acquiring skills to perform an appropriate motor task in response to a sensory cue, e.g. precise reaching with a mouse pointer to a target spot shown on the screen. Motor adaptation is a form of motor learning to overcome movement perturbations caused by novel environment or altered sensory feedback. During motor adaptation, future movements are corrected using error information acquired on previous trials . Representation of the movement error depends on available sensory components. For example, during reaching movements under unexpected perturbation, visual feedback can provide a vector displacement of the movement endpoint relative to the target position. This vector error may be used by the central nervous system to adjust motoneuron activity and eliminate the effects of the perturbed environment. It has been suggested that this process involves the cerebellum that adjusts the internal model of the body based on information about movement error . This type of motor adaptation is often referred to as supervised or error-based learning .
In this study, we modeled the neuromechanical control of reaching movements in humans and used this model to reproduce and explain the results of previous experimental studies demonstrating motor adaptation during reaching [7, 10]. In these experiments the participants did not have direct visual feedback from the arm. Instead, the arm endpoint was represented as a cursor on a display. During each experiment, different targets appeared on the screen and the task was to move the arm so that the cursor would reach the target. Such a setup allowed an experimenter to easily alter the visual feedback if needed. The applied perturbations included image rotations around the movement starting point and reflection across to the vertical axis. In presence of the perturbation, the participants had to learn to reach the target relying on the distorted visual feedback or other available information. To prevent the subjects from making correction during the movement, they were either forced to perform movements as quickly as possible or the cursor was only shown on the screen when the movement was complete.
As previously stated, both basal ganglia and cerebellum may be involved in motor adaptation. Although the functional role of each compartment has been investigated, the interplay between the two structures remains poorly understood . We used mathematical modeling to characterize the functional interactions between these structures during motor adaptation.
The proposed model of motor adaptation to perceptual perturbations includes two distinct learning structures, cerebellum and basal ganglia, responsible for error-based and non-error-based motor learning, respectively. We demonstrate that based on existing experimental evidence, it is necessary to have a mechanism regulating involvement of cerebellum and basal ganglia depending on the perturbation. We suggest that the involvement of a particular learning mechanism is regulated by the same signal depending on the consistency of the internal model used by the brain to predict the movement results. The resulting model reproduces data from several experiments, involving interaction between error-based and non-error-based learning mechanisms.
We distinguish between the model of the motor adaptation system, which is supposed to reproduce activity of some parts of the participant’s brain, and the model of the experimental environment, which is supposed to describe factors and events that the participant does not control. We call the latter “a context”.